RESEARCH/INVESTIGACIÓN

DESCRIPTION OF SOME SPECIES POPULATIONS (NEMATODA) FROM ARGENTINA E. J. Chaves1* and E. A. Mondino2 1NEMA-AGRiS, Laboratorio de análisis de nematodos en suelo y plantas, 1900 La Plata, Argentina; 2Laboratório de Biologia do Solo, Depto. de Solos, Universidade Federal Rural do Rio de Janeiro, BR-465, km 7 Seropédica, 23890- 000 RJ-Brasil. *Corresponding author: [email protected]

ABSTRACT Chaves, E. J., and E. A. Mondino. 2013. Description of some Xiphinema species populations (nematoda) from Argentina. Nematropica 43:68-77. Observations are reported on the morphology and morphometrics of Argentinian populations of Xiphinema krugi, , Xiphinema vulgare and Xiphinema surinamense found in cultivated and uncultivated soils from the Buenos Aires, Santa Fe, Tucumán and Misiones Provinces. Key words: Xiphinema, morphology, morphometrics, cultivated.

RESUMEN Chaves, E. J. and E. A. Mondino. 2013. Descripción de algunas poblaciones de especies de Xiphinema (nematoda) de Argentina. Nematropica 43:68-77. En el presente trabajo son reportadas observaciones morfométricas y morfológicas de poblaciones Argentinas de Xiphinema krugi, X. rivesi, X. vulgare and X. surinamense encontradas en suelos cultivados y no cultivados de las provincias de Buenos Aires, Santa fe, Tucumán y Misiones. Palabras clave: Xiphinema, morfométricas, morfológicas, cultivado.

INTRODUCTION information on the occurrence of Xiphinema species in Argentina is provided in this article. Xiphinema, “the dagger ”, is one of the principal genera of plant parasitic , which MATERIALS AND METHODS is found widely throughout most of the world and is found on all of the continents, except Antarctica. The Soil samples were collected by the first author in economic importance of the genus Xiphinema is related cultivated and uncultivated soils during a survey to the virus vector ability and consequent phytosanitary of plant-parasitic nematodes in several regions of risk of some species, nevertheless, the knowledge on this Argentina between 1978-1980 (Chaves, 1984) and in group of nematodes in Argentina is scarce. Information 1996. Nematodes were extracted with centrifugation- on distribution of these nematodes in Argentina was flotation technique, fixed in hot 4% formaldehyde studied by Luc and Doucet (1990) and Doucet et al. and mounted in pure dehydrated glycerine (de Grisse, (1998), and description of some populations of X. 1969). The specimens were extracted, fixed, measured krugi and X. surinamense from Córdoba and Entre and drawn between 1981-1982 and in 1996. Ríos provinces was provided by Decraemer et al. (1998). The objective of this study was to report our Descriptions observations on the morphology and morphometrics of Argentinian populations of Xiphinema krugi, X. rivesi, Xiphinema krugi Lordello, 1955 X. vulgare and X. surinamense found in cultivated (Table 1-2; Fig. 1, A-H, Fig. 3, B, E); Female (n = 13) and uncultivated soils from the Buenos Aires, Santa Fe, Tucumán and Misiones provinces. Additional Body ventrally arcuate, more or less C-shaped. 68 Description of Xiphinema species from Argentina: Chaves and Mondino 69

Cuticule smooth; internally with transverse striae 0.6 Luc and Hunt (1978) redefinedX. krugi and observed µm. Lateral cord occupying 17% of body width. Lateral a great variation in several biometrical characters. pores usually distinct throughout the body. Dorsal Analysing measurements of the tail and of the anterior and ventral body pores distinct in the anterior body genital branch, they suggested the occurrence of groups region. Head rounded, 6 µm high, 14 µm wide, offset of different geographical origin. Oliveira et al. (2006) by slight constriction. Amphid aperture occupying ½ demonstrated the possibility that X. krugi is a species of head width. Guiding sheath of spear 4-18 µm long, complex comprised of four distinct genotypes and/or its posterior margin 102 µm (94-110) from the anterior cryptic species. Morphometrical data of populations end. Odontophore flanges well developed, 10 µm wide. described here most agrees with PX11 and PX26 Brazil Nerve ring 10-12 µm wide at 209 µm (202-218) from populations (RFLP profile B). the anterior end. Total esophageal length 403 µm (370- 437), the basal bulb of esophagus measuring 94 µm Habitat and localities (85-104) long and 22 µm (20-27) wide. Cardia 10-14 µm long. Hemizonid 6-7 µm wide at 186 µm (173-199) Soil around potato plants in Concepción, Tucumán from the anterior end. Vulva transverse slit, at 736 µm Province; garlic in Médanos and corn in Saladillo, (640-822) from anterior end. Two genital branches, the Buenos Aires Province; strawberry in Coronda, Santa anterior one reduced 92 µm (74-106) long, consisting of Fe Province, collected by E. Chaves 1978-1980. a uterus with distinct large lumen and short pouch-like Eggplant in Helvecia, Santa Fe Province collected by oviduct; between the uterus and oviduct a constriction C. Medera 1979. Table 2 is found formed by a weakly developed sphincter. The posterior genital branch is normally developed 299 µm Xiphinema rivesi Dalmasso, 1969. (202-534) long, consisting of ovary, oviduct, sphincter (Table 3, Fig. 2 A, B, I, Fig. 4); Female (n = 21) and uterus with a wider portion. No spermatozoa, no Z organ. In one female an egg 173 µm long, 43 µm wide Body ventrally arcuate, closed or open C posture, was present near the vagina. Vagina 44-52 % of body tapering toward the extremities. Cuticle smooth, width. Tail conoid with ventral peg of variable length. with 0.6 µm wide transverse striae internally. Lateral Two pairs of caudal pores. Cuticle on tail with minute cord occupying 24-27% of body width. Lateral pores oblique lines. A tail blind terminal canal is present in obscure; dorsal and ventral body pores not seen. Head all specimens. Rectum 37 µm (34-41) long. rounded, almost continuous with the rest of the body, although a slight depression can be noticed. Head 10 Male µm wide. Amphid aperture occupying one half of head Not found. width. Guiding sheat of spear 7.5 µm (6-10) long, posterior margin located at 74 µm (71-79) from anterior Juveniles part of body. Stylet flanges well developed 7 µm (6.5- 8) wide. Nerve ring 8-10 µm wide at 167 µm (153- Resemble females. The elongate tail in the first two 173) from anterior end. Total oesophageal length 338 stages become more conoid and subdigitate in J4 (Fig. µm (314-368); basal bulb 74 µm (70-80) long, 16 µm 1, D-G); Table1 (14-19) wide. Cardia 6-7 µm long. Intestine obscured by lipid granules. Hemizonid 5 µm wide at 141 µm ( Remarks 139-144) from anterior part. Vulva transverse slit, at 985 µm (892-1125) from anterior part. Two genital All the populations of X. krugi here reported are branches, the anterior sligthly shorter or equal to the morphometrically similar to the original description posterior, measuring 157 µm (122-182) and 174 µm (Lordello, 1955) and to the populations described by (145-213), respectively. Uterus small, oviduct simple, Cohn and Sher (1972), Williams and Luc (1977), Luc ovaries reflexed. Sphincter not discernible. Vagina and Hunt (1978), Loof and Sharma (1979), Heyns 23-32% of body width. No Z-organ or spermatozoa. (1977), Ferraz (1980), Ebsary et al. (1984), Oliveira Bacteria present in the ovaries of the all specimens. Tail et al., 2006, and Argentinean populations reported conoid with two pairs of caudal pores. Cuticle on the by Decraemer et al. (1998), and present a tail shape tail with very faint radial striae. An obscure tail blind as shown in figure 1 H. The tail shape of X. krugi canal is present. Prerectum not discernible. Rectum 18 varies from one with a fairly long peg to one without µm (16-20) long. peg (Coomans et al., 2001). The tail is subconoid in original description; regularly ogival with a very Male slight bulge at its extremity to conoid rounded with Not found. distinct ventral peg (Luc and Hunt, 1978); longer with a bluntly knobbed tail terminus and shorter tail with Juveniles rounded terminus in Arkansas and Hawaii populations, Resembles adults in general shape. respectively (Robbins and Ye, 2010). 70 NEMATROPICA Vol. 43, No. 1, 2013

Remarks terminus. Three pairs of caudal pores. Cuticule on the tail with minute oblique lines. Tail blind terminal canal The X. rivesi populations from Argentina show present. Prerectum 502 µm long. Rectum 29 µm long. some differences with respect to the original description (Dalmasso, 1969). In fact, the odontostyle, Male the odontophore and the tail are slightly shorter Not found. and the anterior genital branch is larger than the posterior one in the original description; conversely Juveniles they are similar to the USA populations described Morphologically similar to the adult, except for the by Lamberti and Zacheo (1979) and Wotjowicz et tail length wich is longer in J2 and J3. al. (1982), and the Canada populations described by Ebsary et al., (1984). X. rivesi seems to be the most Remarks widely distributed member of X. americanum group in Argentina, it has a wide host range and is one of Only a female and two juveniles were found. The the five species possessing only three juvenile stages female has similar measurements to both X. vulgare (Robbins et al., 1996). It was synonymized with X. and X. setariae Luc, 1958, but differ however from americanum by Stegarescu (1980), but Wojtowicz et the type of X. vulgare in having shorter odontophore al. (1982) consider X. rivesi as a valid species and add and odontostyle, longer tail length and higher c´ ratio. that the head of X. americanum is slightly offset, its The tail length and c’ value most resemble X. setariae, stylet is shorter and its tail is of a different shape, being but the remaining tail ratios given by Tarjan (1964) more pointed. Later, Georgi (1988) assumed that the are similar to X. vulgare, and the hyaline part of the ratio between the length and diameter of the hyaline extremity of the tail also agrees with X. vulgare. Luc tail tip was useful in distinguishing X. rivesi from X. and Dalmasso (1975) stated that the hyaline tail is the americanum and Alkemade and Loof (1990) stated that most reliable character to separate X. vulgare from X. the tail shape terminus and the anal body diameter are setariae, but such a concept was later rejected by Loof the only valuable characters to differentiate these two and Luc (1990). species. The status of X. vulgare and X. setariae is still controversial. Williams and Luc (1977), Loof and Habitat and locality Sharma (1979), Brown et al. (1981) and Lamberti et al. (1995) support the validity of two species, but Cohn Found in soil around garlic in Los Talas, Berisso, and Sher (1972), Loof and Luc (1990), Heyns and and in alfalfa field in Don Atilio farm, Tandil, Buenos Coomans (1991), and Luc and Baujard (1996) consider Aires province, E. Chaves, 1980 and 1996 respectively. X. vulgare a junior synonym of X. setariae. Table 3 Nevertheless, the tail shape and length and c’ value of female, and tail shape of juveniles from Argentina Xiphinema vulgare Tarjan, 1964. resemble more X. parasetariae Luc, 1958 than the ones (Table 4, Fig. 1, I-L, Fig. 3, A, D); Female of the X. vulgare/X. setariae complex as the original descriptions given by Luc (1958) and descriptions Body arcuate only in the posterior part. Cuticle of X. vulgare given by Brown et al. (1981), and X. smooth; with fine transverse striae internally. Head parasetariae given by Heyns et al. (1994), and Sharma rounded, separated from body by an incisure. Guiding and Siddiqi (1990). According to Lamberti et al., sheath of the odontostyle 14 µm long, its posterior part (2001), because the synonymy of X. vulgare with X. at 101 µm from the anterior end. Odontophore flanges setariae has been proposed by various authors and well developed, 7µm wide. Total esophageal length rejected by others, “to discuss the criteria used by 372 µm; the basal bulb of esophagus measuring 14 x the authors to arrive at their divergent conclusions is 91 µm. Cardia not seen. Esophago-intestinal junction probably unproductive”. not discernible. The anterior part of the intestine forms an evagination on one side of the esophageal bulb. Habitat and locality Nerve ring 7µm wide located 122 µm from anterior extremity. Vulva transverse slit 1220 µm from anterior Found in brackish soil in the Misiones Province extreme. Two genital branches well developed, the (locality unknown), collected by J. Rodriguez 1979. anterior measuring 290 µm long, the posterior one 227 µm long. Uterus with three swollen chambers, two Xiphinema surinamense Loof and Maas, 1972 proximal and one distal, near the oviduct junction. A (Table 5, Fig. 2. C-H, J, Fig. 3, C, F); Female (n = 2) sphincter marks the separation from the oviduct. In the anterior branch the pars dilatata oviductus is only Body ventrally arcuate after fixation, predominantly sligthly swollen, it is more developed in the posterior in the posterior part. Cuticule smooth, with fine branch. No Z-organ or spermatozoa observed. Tail transverse striae internally. Lateral cord occupying uniformly conoid, not clearly digitate, with rounded 16 % of body width. Lateral pores distinct throughout Description of Xiphinema species from Argentina: Chaves and Mondino 71 the body. Dorsal pores distinct in the anterior body Habitat and locality region; the ventral ones distinct throughout the body. Head rounded almost continuous with the rest of the Found in brackish soil associated with X. vulgare in body with a slight depression. Amphidial aperture the Misiones Province (locality unknown) collected by one-half of corresponding head width. Guiding sheath J. Rodriguez 1979. of odontostyle 11-14 µm long; its posterior margin 100-109 µm from anterior extreme. Odontophore flanges well developed 10 µm wide. Total esophageal LITERATURE CITED length 404-407 µm; esophageal bulb 23-24 µm wide, 95-97µm long; cardia 9 µm long. Nerve ring 12 µm Alkemade, J. R. M., and P. A. A. Loof. 1990. The genus wide located 138-149 µm from the anterior extreme. Xiphinema Cobb, 1913 (Nematoda: ) Hemizonid 6 µm wide at 230-318 µm from anterior in Perú. Revue Nématologie, 13:339-348. extreme. Vulva transverse slit, 829-970 µm from Brown, D. J. , M. Luc, and Purbadi. 1981. A anterior extreme. Two genital branches: anterior description of some juveniles stages of Xiphinema branch reduced, without ovary, 275-300 µm long; vulgare (Nematoda:Dorylaimoidea). Nematologia the posterior one is normally developed 430-450 µm Mediterranea, 9:205-210. long, with reflexed ovary. In both branches the uterus Chaves, E. 1984. Observations on plant parasitic is wide with the proximal parts well muscularized; the nematodes from Argentina. PhD. thesis, University distal parts have a vesicular wall. A sphincter is present of Ghent, Belgium, 106 pp. between uterus and oviduct. In the anterior branch the Cohn, E., and S. A. Sher. 1972. A contribution to the oviduct is reduced to a swollen sac. No Z-organ or of the genus Xiphinema Cobb, 1913. sperm visible. One oval egg 54 x 27 µm was present Journal of Nematology, 4:36-65. in the uterus of one specimen. Vagina occupying 1/3 of Coomans, A., R. Huys, J. Heyns and M. Luc. 2001. body width. Tail hemielliptical with two or three pairs Character analysis, phylogeny and biogeography of caudal pores. Cuticle on tail with minute oblique of the genus Xiphinema Cobb, 1913 (Nematoda: lines. One specimen with tail blind terminal canal. Longidoridae). Annales du Musée Royal de Prerectum 225-300 µm long. Rectum 36-42 µm long. l’Afrique Centrale (Zoologie), Tervuren, Belgique, 287:1-239. Male Dalmasso A., 1969. Etude anatomique et Not found. taxonomique des genres Xiphinema, et (Nematoda:). Juveniles Memoires du Museum National d´Histoire Resembles adult in general shape. The tail elongate Naturelle, Ser. A. Zoologie, 61:33-82. in the two first stages becomes more rounded in J3. A Decraemer, W., M. E. Doucet, and A. Coomans. 1998. blind tail terminal canal is clearly visible in J3 and less Longidoridae from Argentina with description visible in J2. The measurements are similar to those of Paraxiphidorus brevistylus sp.n. (Nematoda: given by Loof and Sharma (1979), except for J3 tail Longidoridae). Fundamental and Applied length, that is longer (39 µm vs 30-32 µm). Nematology, 21:371-388. De Grisse, A. 1969. Redescription ou modifications Remarks de quelques techniques utilisées dans l’étude des nématodes phytoparasitaires. Mededelingen The biometrics of the two females from Misiones Rijksfakulteit Landbouwwetenschappen Gent, agree with the original description except for the 34:351-369. shorter stylet and it is more similar to the Brazilian Doucet, M. E., L. C. C. B. Ferraz, J. C. Magunacelaya, population described by Loof and Sharma (1979). and D. J. F. Brown. 1998. The occurrence and There was an egg but sperm were not observed. There distribution of longidorid nematodes in Latin are two caudal pores in the original description, and America. Russian Journal of Nematology, 6:111- two or three in Misiones specimens. The lateral pores, 128. inconspicuous in the original description, are clearly Ebsary, J. W. Potter, and W. R. Allen. 1984. visible on the Argentinean specimens. The structure of Redescription and distribution of Xiphinema rivesi anterior genital branch of Misiones population differs Dalmasso, 1969 and Cobb, from the others Argentinean populations described by 1913 in Canada with a description of Xiphinema Decraemer et al. (1998) in having a well demarcated occiduum n. sp. (Nematoda: Longidoridae). ovejector from the glandular part of the uterus and in Canadian Journal of Zoology, 62:1696-1702. lacking cristalloid structures. However the anterior Ferraz, L. C. B., 1980. Observations on some uterus of the Misiones population close resembles the Xiphinema species found in Brazil (Nematoda: paratype illustrated by Decraemer et al. (1998). Dorylaimoidea). Nematologia Mediterranea, 8:141- 151. 72 NEMATROPICA Vol. 43, No. 1, 2013

Fig. 1. Xiphinema krugi: A, female anterior region; B, amphid shape; C, female anterior genital branch; D-H, tail of J1, J2, J3, J4 and female respectively. X. vulgare: I-K, tail of J2 , J3 and female respectively; L, female anterior region. Description of Xiphinema species from Argentina: Chaves and Mondino 73

Fig. 2. Xiphinema rivesi: A, female anterior region; B, female tail. X. surinamense: C, female anterior genital branch; D-F, tail of J1, J2 and J3 respectively; G, female anterior region; H, female tail; I-J, amphid shape of X. rivesi and X. surinamense, respectively. 74 NEMATROPICA Vol. 43, No. 1, 2013 female , female B, D A, C

Xiphinema rivesi Xiphinema Fig. 4. Photomicrographs of population, of garlic region and posterior anterior bars Scale population. of lucerne region and posterior anterior = 20 µm. = X. D ), A, D ( = 20µm, X. vulgare A, B, C, F, E A, B, C, F, ). Scale bars: ). Scale B, E ( krugi

Xiphinema ) and C, F ( Fig. 3. Photomicrographs of anterior and posterior regions surinamense 50 µm. Description of Xiphinema species from Argentina: Chaves and Mondino 75

Table 1. Morphometrics of females of Xiphinema krugi from different populations in Argentina Concepción Helvecia Coronda Saladillo Médanos n 3 4 1 4 1 L (mm) 2.20 2.20 2.37 2.14 2.23 (2.10-2.23) (2.00-2.34) (2.00-2.225) a 48 47 49 50.7 48 (46.7-49.6) (42.5-50) (50-51) b 5.5 5.1 6.3 5.4 5.6 (5.2-6.0) (4.9-5.4) (5.2-5.7) c 61 55 55 58 54 (57-67) (52-60) (55-62) c´ 1.0 1.3 1.5 1.2 1.3 (1.0-1.1) (1.1-1.4) (1.2-1.3) V 34.6 33.7 34 32 33 (34-35) (33-35) (31-33) Odontostyle (µm) 112 108 110 105 103 (111-113) (106-111) (103-108) Odontophore (µm) 70 71.7 64 68.5 68 (71.73) (67-70) Stylet (µm) 182 180 174 174 171 (181-183) (178-182) (173-178) Tail length 35 39.5 43 37 41 (33-37) (39-41) (36-38) Anterior genital branch/vulval diameter 1.6 2.3 2.0 2.0 2.0 (1.8-2.4) n = number of specimens; L = body length; a = body length/body width; b = body length/distance from anterior end to end of pharynx; c = body length/tail length; c’ = tail length/ body width at anus or cloaca; V = distance from anterior end to vulva x 100/ body length.

Table 2. Morphometrics of juveniles of Xiphinema krugi J1 J2 J3 J4 n 2 8 16 9 L (mm) 0.69-0.77 1.05 1.31 1.75 (0.93-1.12) (1.19-1.48) (1.56-1.91) a 34.5-37.5 37 41.7 45.4 (34-40) (37-47) (43-49) b 3.2-3.4 3.8 4 4.7 (3.2-4.2) (3.5-4.8) (4-5.5) c 18-19 23.6 29 41 (23-25) (25-34) (39-45) c´ 2.5-3.0 2.1 1.8 1.4 (1.9-2.5) (1.6-2.4) (1.3-1.6) Odontostyle 46 58 76 92 (57-59) (71-80) (89-96) Odontophore 33-35 45 51 61 (43-46) (47-54) (58-64) Stylet 79-81 103 127 153 (100-105) (120-132) (151-156) Replacement ondontostyle 57 77 91 107 (74-79) (87-96) (99-116) Tail 39-42 44 44 43 (39-47) (41-50) (36-48) n = number of specimens; L = body length; a = body length/body width; b = body length/distance from anterior end to end of pharynx; c = body length/tail length; c’ = tail length/body width at anus or cloaca; V = distance from anterior end to vulva x 100/body length. 76 NEMATROPICA Vol. 43, No. 1, 2013

Table 3. Measurements of Xiphinema rivesi from Argentina Population Los Talas Population Tandil Female J2 Female J2 J3 n 10 2 11 1 5 L (mm) 1.85 1.46-1.56 1.93 1.10 1.43 (1.68-2.10) (1.71-2.04) (1.38-1.47) a 42 43-44 51 46 45-54z (38-48) (45-54) b 5.4 4.75-5.0 6.2 3.8 4.8 (5-6) (5.7) (4.7-5.0) c 59 43-47 60 33 42.5 (53-66) (54-66) (39-46) c´ 1.3 1.5-1.6 1.5 2.3 1.9 (1.2-1.5) (1.4-1.8) (1.8-2.1) V 53 - 53.4 - - (51-54) (52-56) Odontostyle (µm) 91 68-75 92 55 71 (86-97) (87-97) (69-73) Odontophore (µm) 47 40-41 48 37 42y (44-51) (45-51) (39-45) Stylet (µm) 138 108-116 141 92 112y (132-148) (135-148) (110-117) Replacement - odontostylet (µm) - 86-89 - 71 90 (86-95) Tail length (µm) 31 33-34 32 33 33.5 (30-34) (30-35) (31.36) n = number of specimens; L = body length; a = body length/body width; b = body length/distance from anterior end to end of pharynx; c = body length/tail length; c’ = tail length/body width at anus or cloaca; V = distance from anterior end to vulva x 100/body length. zn = 2, yn = 3

Table 4. Measurements of Xiphinema vulgare from Table 5. Measurements of Xiphinema surinamense from Argentina Argentina Female J2 J3 Female J1 J2 J3 n 1 2 1 n 2 1 1 1 L 2.98 1.12-1.20 1.60 L 2.22-2.46 0.73 0.89 1.16 a 65 46-47 59 a 43-48 41 37 39 b 8 4.3-4.6 5 b 5.4-6 3 3.6 3.7 c 46 16-16.5 20.6 c 72 17.5 25 29.5 c´ 2.5 4.2-4.3 4.3 c´ 0.8-0.9 3.2 1.9 1.7 V 41 - - V 37-39 - - - Odontostyle 105 61 74 Odontostyle 103-108 46 51 70 Odontophore 60 38-41 49 Odontophore 72-76 37 42 54 Stylet 165 99-102 123 Stylet 175-184 83 93 124 Replacement odontostyle - 74-76 91 Replacement odontostyle - 57 67 86 Tail 65 70-73 79 Tail 32-34 42 36 39 LNT 18 8-9 16 n = number of specimens; L = body length; a = body length/ Tail/LNT 3.6 7.7-9 4.8 body width; b = body length/distance from anterior end to n = number of specimens; L = body length; a = body end of pharynx; c = body length/tail length; c’ = tail length/ length/body width; b = body length/distance from body width at anus or cloaca; V = distance from anterior anterior end to end of pharynx; c = body length/tail end to vulva x 100/body length. length; c’ = tail length/body width at anus or cloaca; V = distance from anterior end to vulva x 100/body length; LNT length of the hyaline part of tail. Description of Xiphinema species from Argentina: Chaves and Mondino 77

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